Molecular mechanisms of microbial interactions in model systems and natural environments

Abstract

Marine microbes are dominant life forms in the ocean and comprise dynamic populations of viruses, bacteria, archaea and single-celled eukaryotes. Interactions between marine microbes impact global biogeochemical cycles and form the base of marine food webs. Interactions range from symbiotic to parasitic, and are mediated through nutrient exchanges and chemical signals. In this dissertation, I focus on characterizing molecular mechanisms responsible for interactions within two groups of microorganisms, phytoplankton and bacteria. In Chapter 1, I studied how extracellular metabolites of an antagonistic bacterium Croceibacter atlanticus impact physiological and transcriptional changes in the model diatom Thalassiosira pseudonana through lab co-culture experiments. In response to extracellular bacterial metabolites, T. pseudonana showed inhibition of cell division, with transcriptional changes in cell cycle regulation, amino acid production and cell wall stability, suggesting that bacterial metabolites may modulate diatom metabolism in ways that support bacterial growth. In Chapter 2, I developed a new statistical method to detect microbial interactions and their transcriptional signatures from environmental metatranscriptome data collected in the North Pacific. Most consistent transcriptional interactions occurred in cross-kingdom pairs especially between diatoms and Proteobacteria, ranging from common functional mechanisms like cross-feeding and defense to species-specific mechanisms occurring through secondary metabolite exchanges, revealing molecular mechanisms of interactions directly in natural communities. In Chapter 3, I studied metabolic capabilities and interactions of 52 novel heterotrophic bacteria isolates capable of utilizing phytoplankton-derived organic matter from the Equatorial Pacific. I generated and analyzed closed genomes of novel strains, species and genus, and proposed potential metabolic exchanges between bacteria including cross-feeding of vitamins and growth factors that may influence interactions with phytoplankton hosts. In Chapter 4, I designed a course-based undergraduate research experience (CURE) that teaches students laboratory techniques and data analysis skills in genomics through exploration of the metabolism of marine bacteria. Novel Equatorial Pacific isolates and their genomes were used by students in their independent research projects to determine capacity of bacteria to grow on select phytoplankton metabolites and connect the growth phenotype to the genomic capability of the bacteria. This dissertation provides insights into the molecular mechanisms controlling interactions in marine microbial communities, from controlled lab studies to natural environments, and introduces novel methodologies to help advance our understanding of microbial interactions.